The Effects of an Arbuscular Mycorrhizal Fungus and Rhizobium Symbioses on Soybean Aphid Mostly Fail to Propagate to the Third Trophic Level

Abstract

The cascading effects of microbe–plant symbioses on the second trophic level, such as phytophagous insects, have been most studied. However, few studies have examined the higher third trophic level, i.e., their natural enemies. We investigated the effects of the symbiotic associations between an arbuscular mycorrhizal (AM) fungus, Rhizophagus irregularis (Glomerales: Glomeraceae), a nitrogen-fixing bacterium, Bradyrhizobium japonicum (Rhizobiales: Bradyrhizobiaceae), and soybean, Glycine max (L.) Merr. (Fabaceae) on two natural enemies of the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), the ladybird beetle Coleomegilla maculata (De Geer) (Coleoptera: Coccinellidae), and the parasitoid Aphelinus certus Yasnosh (Hymenoptera: Aphelinidae). We measured the growth and survival in the predator and parasitoid reared on aphids feeding on soybean inoculated seedlings. The rhizobium symbiosis alone was affected with a decreased rate of parasitoid emergence, presumably due to decreased host quality. However, number of mummies, sex-ratio, development time, and parasitoid size were all unaffected by inoculation. AM fungus alone or co-inoculated with the rhizobium was unaffected with any of the parameters of the parasitoid. For the predator, none of the measured parameters was affected with any inoculant. Here, it appears that whatever benefits the microbe–plant symbioses confer on the second trophic level are little transferred up to the third.